The contribution of cell-cell signaling and motility to bacterial biofilm formation

Shrout, Joshua D.; Tolker‐Nielsen, Tim; Givskov, Michael; Parsek, Matthew R.

doi:10.1557/mrs.2011.67

Cited by 97 publications

(75 citation statements)

References 55 publications

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“…Since translocation on surfaces has important consequences with respect to surface colonization, this mechanism suggests a new strategy for community architecture development and subsequent biofilm formation (44). This and earlier work by O'Toole's laboratory (45) demonstrate key roles for P. aeruginosa flagellar motors in these processes.…”

mentioning

confidence: 52%

Fifty Ways To Inhibit Motility via Cyclic Di-GMP: the Emerging Pseudomonas aeruginosa Swarming Story

McCarter

Gomelsky

2014

J. Bacteriol.

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) offer a new, previously unseen way of swarming motility inhibition in Pseudomonas aeruginosa PA14. This bacterium possesses a single flagellum with one rotor and two sets of stators, only one of which can provide torque for swarming. The researchers discovered that elevated levels of c-di-GMP inhibit swarming by skewing stator selection in favor of the nonfunctional, "bad" stators.A seemingly bizarre way to inhibit motility. Since its discovery in the 1980s (1) and its very humble beginnings, cyclic dimeric GMP (c-di-GMP) has risen to the limelight of bacterial signal transduction as one of the most common bacterial second messengers (2). While c-di-GMP signaling pathways affect various aspects of bacterial physiology and metabolism, perhaps the best-known processes are the transition of motile bacteria to the nonmotile, sessile state and the regulation of biofilm formation. c-di-GMP inhibits motility via many mechanisms, most of which remain poorly understood. The study by the O'Toole and Armitage groups in this issue of the Journal of Bacteriology offers a new, previously unseen twist on c-di-GMP-dependent swarming motility control in Pseudomonas aeruginosa PA14 (3). This bacterium possesses dual flagellar motors that function under different conditions. The researchers discovered that elevated levels of c-di-GMP stop swarming by affecting stator selection. Stators are the proton-conducting membrane channels that generate torque, which powers flagellar rotation. Removing high-functioning stators and allowing the "bad" ones that do not support swarming motility to stay seems like a very strange way to stop. To put this study in perspective, let us take a closer look at the structures and functions of flagella, at the various stator arrangements, and at the ways and means by which c-di-GMP is known to affect flagellar functions.Diversity in flagellar organization and function. Flagellar propelled motility is a very effective and widespread mode of microbial locomotion. The types of flagella and their arrangement on the cell body and the motors, the energy sources, and the chemotactic navigation systems found in microbes are amazingly diverse (4). Flagella can be single polar, multiple tufted polar, sheathed polar, peritrichous (around), lateral (near but not at a pole), and even periplasmic. The same flagella often propel bacteria in lowviscosity and relatively high-viscosity media, but this is possible only up to a point (5). Under conditions of high load, i.e., very high viscosity or on a solid surface, flagellar performance diminishes. To aid motility, some bacteria employ performance-enhancing stratagems. For example, representatives from Aeromonas, Azospirillum, Shewanella, and Vibrio use a distinct second flagellar system optimized for swarming over a surface, whereas Proteus greatly increases flagellar numbers to permit surface translocation (reviewed in references 6 and 7). Yet other bacteria elegantly engage new motor parts to accommodate changing demands (reviewed in reference 8).Flagella are turned ...

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mentioning

confidence: 52%

Fifty Ways To Inhibit Motility via Cyclic Di-GMP: the Emerging Pseudomonas aeruginosa Swarming Story

McCarter

Gomelsky

2014

J. Bacteriol.

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“…Cells move along the ECM through focal adhesions and specific recognition of ECM components. In bacteria, the ECM also promotes extracellular recognition, adhesion, and motility, allowing the formation of antibiotic-resistant biofilms (2). Therefore, functional studies of the ECM have received attention in many fields from cancer biology to bacteriology.…”

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confidence: 99%

“…However, the role of slime has never been addressed directly, leaving its propulsive contribution as an open question. Slime could also facilitate motility, promoting specific adhesion and allowing cellcell communication through the deposition of signaling molecules (2). In the past, slime has been observed by invasive techniques such as EM, nonspecific staining, or DIC on glass (6, 9) (see below), which prevented its analysis during the motility of live cells.…”

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confidence: 99%

Wet-surface–enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility

Ducret

Valignat

Mouhamar

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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In biology, the extracellular matrix (ECM) promotes both cell adhesion and specific recognition, which is essential for central developmental processes in both eukaryotes and prokaryotes. However, live studies of the dynamic interactions between cells and the ECM, for example during motility, have been greatly impaired by imaging limitations: mostly the ability to observe the ECM at high resolution in absence of specific staining by live microscopy. To solve this problem, we developed a unique technique, wet-surface enhanced ellipsometry contrast (Wet-SEEC), which magnifies the contrast of transparent organic materials deposited on a substrate (called Wet-surf) with exquisite sensitivity. We show that Wet-SEEC allows both the observation of unprocessed nanofilms as low as 0.2 nm thick and their accurate 3D topographic reconstructions, directly by standard light microscopy. We next used Wet-SEEC to image slime secretion, a poorly defined property of many prokaryotic and eukaryotic organisms that move across solid surfaces in absence of obvious extracellular appendages (gliding). Using combined Wet-SEEC and fluorescent-staining experiments, we observed slime deposition by gliding Myxococcus xanthus cells at unprecedented resolution. Altogether, the results revealed that in this bacterium, slime associates preferentially with the outermost components of the motility machinery and promotes its adhesion to the substrate on the ventral side of the cell. Strikingly, analogous roles have been proposed for the extracellular proteoglycans of gliding diatoms and apicomplexa, suggesting that slime deposition is a general means for gliding organisms to adhere and move over surfaces.label-free imaging | microfluidic I n mammals, cell migrations are essential for many developmental processes, for example during embryogenesis when the neural crest is formed and also during pathologies at the onset of the immune response or cancer metastasis (1). In these processes, the extracellular matrix (ECM) provides support and anchorage for cells, allowing local tissue differentiation and regulating intercellular communications (1). In general the ECM has a complex composition of polysaccharide gels (glycosaminoglycans) and fibrous proteins. Cells move along the ECM through focal adhesions and specific recognition of ECM components. In bacteria, the ECM also promotes extracellular recognition, adhesion, and motility, allowing the formation of antibiotic-resistant biofilms (2). Therefore, functional studies of the ECM have received attention in many fields from cancer biology to bacteriology.Historically, electron microscopy has been the method of choice to image the structure of the ECM at high resolution. However, this method requires fixation procedures and does not allow studies of the ECM under live conditions. In general, live imaging approaches have used optical fluorescence microscopy and specific stains (i.e., antibodies, lectins) to localize specific components of the ECM, a polysaccharide or a given protein.A major limitation wi...

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“…The studies from Lehner et al (2005) demonstrated the ability of biofilm-producing strains of C. sakazakii to synthesize the cell signalling molecules acyl homoserine lactones (AHLs), which mediate quorum sensing (QS). This cell-to-cell signalling along with other genetic and environmental factors have been reported to be involved in biofilm formation in bacteria (Waters & Bassler, 2005;Shrout et al, 2011). Therefore, the interference with this phenomenon by means of quorum-sensing inhibitor (QSI) could be an attractive approach to prevent or to reduce biofilm-based infections.…”

Section: Introductionmentioning

confidence: 99%

Inhibition of quorum-sensing-mediated biofilm formation in Cronobacter sakazakii strains

et al. 2016

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The present study investigated plant extracts for their anti-quorum-sensing (QS) potential to inhibit the biofilm formation in Cronobacter sakazakii strains. The bioassay based on loss of pigment production by Chromobacterium violaceum 026 and Agrobacterium tumefaciens NTL4 (pZLR4) was used for initial screening of the extracts. Further, the effect of extracts on the inhibition of QS-mediated biofilm in C. sakazakii isolates was evaluated using standard crystal violet assay. The effect on biofilm texture was studied using SYTO9 staining and light and scanning electron microscopy. Among the tested extracts, Piper nigrum and Cinnamomum verum at 100 ppm resulted in 78 and 68 % reduction in the production of violacein as well as blue-green colour in both biosensor strains. A higher inhibitory activity (>50 %) on biofilm formation in C. sakazakii was observed for Pip. nigrum and Cin. verum, whereas the other extracts possessed moderate (25-50 %) and minimal (<25 %) inhibitory activities. Further, the fluorescent and scanning electron microscopic images indicated a major disruption in the architecture of biofilms of tested strains by Pip. nigrum. This study points to the possibility of using Pip. nigrum and Cin. verum as inhibitor of QS-mediated biofilm formation by C. sakazakii that could be further explored for novel bioactive molecules to limit the emerging infections of C. sakazakii.

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The contribution of cell-cell signaling and motility to bacterial biofilm formation

Cited by 97 publications

References 55 publications

Fifty Ways To Inhibit Motility via Cyclic Di-GMP: the Emerging Pseudomonas aeruginosa Swarming Story

Fifty Ways To Inhibit Motility via Cyclic Di-GMP: the Emerging Pseudomonas aeruginosa Swarming Story

Wet-surface–enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility

Inhibition of quorum-sensing-mediated biofilm formation in Cronobacter sakazakii strains

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